Thrombospondin-1 is a novel negative regulator of liver regeneration after partial hepatectomy through transforming growth factor-beta1 activation in mice

Hepatology

Volumn 55, Issue 5, 2012, Pages 1562-1573

  Hayashi, Hiromitsu ^a   Sakai, Keiko ^a   Baba, Hideo ^b   Sakai, Takao ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b KUMAMOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN; CYCLIN A2; CYCLIN D1; PROTEIN P21; REACTIVE OXYGEN METABOLITE; SMAD PROTEIN; STAT3 PROTEIN; THROMBOSPONDIN 1; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL CYCLE S PHASE; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; IMMEDIATE EARLY GENE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LIPID PEROXIDATION; LIVER CELL; LIVER REGENERATION; MALE; MOUSE; NONHUMAN; PARTIAL HEPATECTOMY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; DEOXYURIDINE; DISEASE MODELS, ANIMAL; DOWN-REGULATION; HEPATECTOMY; IMMUNOHISTOCHEMISTRY; LIPID PEROXIDATION; LIVER REGENERATION; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; RANDOM ALLOCATION; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; THROMBOSPONDIN 1; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84859947735     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.24800     Document Type: Article

References (36)

1. Taub R. Liver regeneration 4: transcriptional control of liver regeneration. FASEB J 1996; 10: 413-427.
2. Fausto N. Liver regeneration. J Hepatol 2000; 32: 19-31.
3. McMahon JB, Richards WL, de Campo AA, Song MK, Thorgeirsson SS. Differential effects of transforming growth factor-beta on proliferation of normal and malignant rat liver epithelial cells in culture. Cancer Res 1986; 46: 4665-4671.
4. Michalopoulos GK. Liver regeneration. J Cell Physiol 2007; 213: 286-300.
5. Jakowlew SB, Mead JE, Danielpour D, Wu J, Roberts AB, Fausto N. Transforming growth factor-beta (TGF-beta) isoforms in rat liver regeneration: messenger RNA expression and activation of latent TGF-beta. Cell Regul 1991; 2: 535-548.
6. Braun L, Mead JE, Panzica M, Mikumo R, Bell GI, Fausto N. Transforming growth factor beta mRNA increases during liver regeneration: a possible paracrine mechanism of growth regulation. Proc Natl Acad Sci U S A 1988; 85: 1539-1543.
7. Oe S, Lemmer ER, Conner EA, Factor VM, Levéen P, Larsson J, et al. Intact signaling by transforming growth factor beta is not required for termination of liver regeneration in mice. HEPATOLOGY 2004; 40: 1098-1105.
8. Mosher DF. Physiology of thrombospondin. Annu Rev Med 1990; 41: 85-97.
9. Crawford SE, Stellmach V, Murphy-Ullrich JE, Ribeiro SM, Lawler J, Hynes RO, et al. Thrombospondin-1 is a major activator of TGF-beta1 in vivo. Cell 1998; 93: 1159-1170.
10. Adams JC. Thrombospondins: multifunctional regulators of cell interactions. Annu Rev Cell Dev Biol 2001; 17: 25-51.
11. Kyriakides TR, Maclauchlan S. The role of thrombospondins in wound healing, ischemia, and the foreign body reaction. J Cell Commun Signal 2009; 3: 215-225.
12. Lawler J, Sunday M, Thibert V, Duquette M, George EL, Rayburn H, Hynes RO. Thrombospondin-1 is required for normal murine pulmonary homeostasis and its absence causes pneumonia. J Clin Invest 1998; 101: 982-992.
13. Moriya K, Bae E, Honda K, Sakai K, Sakaguchi T, Tsujimoto I, et al. A fibronectin-independent mechanism of collagen fibrillogenesis in adult liver remodeling. Gastroenterology 2011; 140: 1653-1663.
14. Yuan H, Zhang H, Wu X, Zhang Z, Du D, Zhou S, et al. Hepatocyte-specific deletion of Cdc42 results in delayed liver regeneration after partial hepatectomy in mice. HEPATOLOGY 2009; 49: 240-249.
15. Yoshie M, Nishimori H, Lee GH, Ogawa K. High colony forming capacity of primary cultured hepatocytes as a dominant trait in hepatocarcinogenesis-susceptible and resistant mouse strains. Carcinogenesis 1998; 19: 1103-1107.
16. Ribeiro SM, Poczatek M, Schultz-Cherry S, Villain M, Murphy-Ullrich JE. The activation sequence of thrombospondin-1 interacts with the latency-associated peptide to regulate activation of latent transforming growth factor-beta. J Biol Chem 1999; 274: 13586-13593.
17. Meek RL, Cooney SK, Flynn SD, Chouinard RF, Poczatek MH, Murphy-Ullrich JE, Tuttle KR. Amino acids induce indicators of response to injury in glomerular mesangial cells. Am J Physiol Renal Physiol 2003; 285: F79-F86.
18. Asai K, Tamakawa S, Yamamoto M, Yoshie M, Tokusashi Y, Yaginuma Y, et al. Activated hepatic stellate cells overexpress p75NTR after partial hepatectomy and undergo apoptosis on nerve growth factor stimulation. Liver Int 2006; 26: 595-603.
19. Breitkopf K, Sawitza I, Westhoff JH, Wickert L, Dooley S, Gressner AM. Thrombospondin 1 acts as a strong promoter of transforming growth factor beta effects via two distinct mechanisms in hepatic stellate cells. Gut 2005; 54: 673-681.
20. Albrecht JH, Poon RYC, Ahonen CL, Rieland BM, Deng C, Crary GS. Involvement of p21 and p27 in the regulation of CDK activity and cell cycle progression in the regenerating liver. Oncogene 1998; 16: 2141-2150.
21. Westerhausen DR, Jr. Hopkins WE, Billadello JJ. Multiple transforming growth factor-beta-inducible elements regulate expression of the plasminogen activator inhibitor type-1 gene in Hep G2 cells. J Biol Chem 1991; 266: 1092-1100.
22. Lee FY, Li Y, Zhu H, Yang S, Lin HZ, Trush M, Diehl AM. Tumor necrosis factor increases mitochondrial oxidant production and induces expression of uncoupling protein-2 in the regenerating mice [correction of rat] liver. HEPATOLOGY 1999; 29: 677-687.
23. Kaur S, Martin-Manso G, Pendrak ML, Garfield SH, Isenberg JS, Roberts DD. Thrombospondin-1 inhibits VEGF receptor-2 signaling by disrupting its association with CD47. J Biol Chem 2010; 285: 38923-38932.
24. Taub R. Liver regeneration: from myth to mechanism. Nat Rev Mol Cell Biol 2004; 5: 836-847.
25. Nakatani T, Inouye M, Mirochnitchenko O. Overexpression of antioxidant enzymes in transgenic mice decreases cellular ploidy during liver regeneration. Exp Cell Res 1997; 236: 137-146.
26. Tomomura A, Sawada N, Sattler GL, Kleinman HK, Pitot HC. The control of DNA synthesis in primary cultures of hepatocytes from adult and young rats: interactions of extracellular matrix components, epidermal growth factor, and the cell cycle. J Cell Physiol 1987; 130: 221-227.
27. Ning M, Sarracino DA, Kho AT, Guo S, Lee SR, Krastins B, et al. Proteomic temporal profile of human brain endothelium after oxidative stress. Stroke 2011; 42: 37-43.
28. Ding BS, Nolan DJ, Butler JM, James D, Babazadeh AO, Rosenwaks Z, et al. Inductive angiocrine signals from sinusoidal endothelium are required for liver regeneration. Nature 2010; 468: 310-315.
29. Zhang X, Lawler J. Thrombospondin-based antiangiogenic therapy. Microvasc Res 2007; 74: 90-99.
30. Albrecht JH, Meyer AH, Hu MY. Regulation of cyclin-dependent kinase inhibitor p21(WAF1/Cip1/Sdi1) gene expression in hepatic regeneration. HEPATOLOGY 1997; 25: 557-563.
31. Annes JP, Munger JS, Rifkin DB. Making sense of latent TGFbeta activation. J Cell Sci 2003; 116: 217-224.
32. Shimizu M, Hara A, Okuno M, Matsuno H, Okada K, Ueshima S, et al. Mechanism of retarded liver regeneration in plasminogen activator-deficient mice: impaired activation of hepatocyte growth factor after Fas-mediated massive hepatic apoptosis. HEPATOLOGY 2001; 33: 569-576.
33. Chen RH, Su YH, Chuang RL, Chang TY. Suppression of transforming growth factor-beta-induced apoptosis through a phosphatidylinositol 3-kinase/Akt-dependent pathway. Oncogene 1998; 17: 1959-1968.
34. Chen RH, Chang MC, Su YH, Tsai YT, Kuo ML. Interleukin-6 inhibits transforming growth factor-beta-induced apoptosis through the phosphatidylinositol 3-kinase/Akt and signal transducers and activators of transcription 3 pathways. J Biol Chem 1999; 274: 23013-23019.
35. Sun J, Hopkins BD, Tsujikawa K, Perruzzi C, Adini I, Swerlick R, et al. Thrombospondin-1 modulates VEGF-A-mediated Akt signaling and capillary survival in the developing retina. Am J Physiol Heart Circ Physiol 2009; 296: H1344-H1351.
36. Wang Y, Wang S, Sheibani N. Enhanced proangiogenic signaling in thrombospondin-1-deficient retinal endothelial cells. Microvasc Res 2006; 71: 143-151.